First Record of Monocorophium Uenoi (Stephenson, 1932) (Crustacea: Amphipoda: Corophiidae) in the Bay of Biscay, French Atlantic Coast
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BioInvasions Records (2019) Volume 8, Issue 1: 87–95 CORRECTED PROOF Rapid Communication First record of Monocorophium uenoi (Stephenson, 1932) (Crustacea: Amphipoda: Corophiidae) in the Bay of Biscay, French Atlantic coast Benoit Gouillieux1,* and Cécile Massé2 1Université de Bordeaux, Station Marine d’Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France 2UMS 2006 AFB-MNHN-CNRS Patrimoine Naturel, Station Marine d’Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France Author e-mails: [email protected] (BG), [email protected] (CM) *Corresponding author Citation: Gouillieux B, Massé C (2019) First record of Monocorophium uenoi Abstract (Stephenson, 1932) (Crustacea: Amphipoda: Corophiidae) in the Bay of The non-indigenous amphipod Monocorophium uenoi was recorded for the first Biscay, French Atlantic coast. time on the French Atlantic coast. This species has been collected in Arcachon Bay BioInvasions Records 8(1): 87–95, and Bidasoa Estuary as early as 2007, probably introduced with non-native oysters. https://doi.org/10.3391/bir.2019.8.1.09 A summary on its morphological characters and its current distribution is done, and Received: 30 April 2018 an updated identification key to Monocorophium species for European waters is Accepted: 16 October 2018 provided. Published: 12 February 2019 Key words: non-indigenous species, Peracarida, Corophiini, Arcachon Bay, Bidasoa Thematic editor: Cynthia McKenzie Estuary, Pacific oyster Copyright: © Gouillieux and Massé This is an open access article distributed under terms of the Creative Commons Attribution License Introduction (Attribution 4.0 International - CC BY 4.0). OPEN ACCESS. The genus Monocorophium Bousfield and Hoover, 1997 is represented by 4 species in European waters: M. acherusicum (Costa, 1853), M. insidiosum (Crawford, 1937), M. sextonae (Crawford, 1937) and M. uenoi (Stephenson, 1932) (Lincoln 1979; Bousfield and Hoover 1997; Faasse 2014). These species are native from European waters, except M. uenoi native from Japan, and M. sextonae which may have a South-West Pacific origin for some authors (Goulletquer et al. 2002). M. uenoi was recorded in The Netherlands in 2013 (Faasse 2014) – the first report from European waters. The present paper deals with M. uenoi record from the French Atlantic coast, which precedes the previous record. Materials and methods Study area (Figure 1) Arcachon Bay is a 180 km² macrotidal coastal lagoon, connected to the Atlantic Ocean by a narrow channel and receives freshwater from Leyre River. The lagoon is characterized by large intertidal flats (115 km²) (Plus et al. 2010). Farms rearing the Pacific oyster Magallana gigas (Thunberg, 1793) occupy the deeper intertidal. Between 2007 and 2017, water temperature Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 87 First record of Monocorophium uenoi in the Bay of Biscay Figure 1. Locations in Europe with records of Monocorophium uenoi. NL: The Netherlands. AB: Arcachon Bay. BE: Bidasoa Estuary. Black spot: Faasse 2014. Red stars: present study. ranged from 4 to 25 °C and salinity ranged from 21 to 36 with an average of 16 ± 4 °C and 33 ± 2 (mean ± SD) respectively. Bidasoa Estuary represents the border between France and Spain in the South East of the Bay of Biscay. It is a short estuary with some feral oyster reefs. No shellfish or commercial port are present. Water temperature ranged from 12 to 22 °C and salinity ranged from 13 to 35 ppt with an average of 17 ± 4 °C and 31 ± 5 (mean ± SD) respectively. Environmental data (temperature and salinity) for both Arcachon Bay and Bidasoa Estuary were provided by the SOMLIT (Sevice d’Observation en Milieu LITtoral, a French coastal monitoring network: http://somlit. epoc.u-bordeaux1.fr/fr/). Material examined Monocorophium uenoi was collected during benthic surveys, in Arcachon Bay and Bidasoa Estuary (Figure 1, Table 1). Specimens were examined with a Nikon SMZ 1500 stereomicroscope and a Nikon Eclipse E400 microscope with up to 112,5 and 400x magnifications (and transmitted light) respectively. Body length (BL) was measured with NIS-Elements Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 88 First record of Monocorophium uenoi in the Bay of Biscay Table 1. Sampling details. N = number of specimens of Monocorophium uenoi collected in Pacific oyster reef. Site Station Latitude Longitude Date N MNHN depository MNHN-IU-2016-3430 Arcachon Bay Les Hosses 44.666667 −1.166667 May 2007–June 2008 135* (25 specimens) – Jacquet 44.666667 −1.083333 July 2014 26 – Arguin 44.583333 −1.233333 December 2017 6 – La Nègue 44.666667 −1.133333 September 2015 1 MNHN-IU-2016-3429 – Ile aux oiseaux Nord 44.683333 −1.166667 September 2015 20 (5 specimens) MNHN-IU-2016-3428 Bidasoa Estuary Station nautique 43.366667 −1.766667 October 2015 50 (20 specimens) * Specimens collected during Salvo (2010) thesis. Analysis software from the anterior margin of head to the posterior end of telson. For Scanning Electron Microscope (SEM) studies, specimens were dehydrated in a graded ethanol series, critical point dried, sputter coated with gold and examined with a Hitachi TM3030Plus scanning electron microscope. Some specimens were deposited in the Muséum National d’Histoire Naturelle (MNHN, Paris) (Table 1). Results Out of 238 specimens of Monocorophium uenoi collected, 72% were females, including ovigerous individuals, and 28% were males. Both in Arcachon Bay and Bidasoa Estuary, specimens were all collected in oyster reefs (Magallana gigas) between May 2007 and December 2017 (see Table 1). Diagnose of male Monocorophium uenoi from Arcachon Bay (SW France) (Figure 2) Rostrum short, projecting slightly beyond lateral head lobes. Antenna 1 peduncle article 1 without lateral and with 3 ventral robust setae, without ventromedial process. Antenna 2 peduncle article 3 without robust seta; article 4 with 1 ventromedial robust seta and distoventral bidentate tooth; article 5 without robust seta, with 1 proximoventral and 1 distomedial process. Gnathopod 1 dactylus longer than palmar margin. Gnathopod 2 dactylus with 3 ventral teeth (tip of dactylus not counted as tooth). Urosome segment 1–3 fused. Uropod 1 inserted mainly laterally from lateral notches; peduncle with 1 distomedial robust seta. Uropod 2 inner ramus outer margin bare. Telson with 3 proximolateral setae and with 2 row of 4 robust setae tooth-like on the dorsodistal depression. Female Sexually dimorphic characters based on adult females, Arcachon Bay (SW France), (Figure 3A–C). Rostrum shorter, not exceeding lateral head lobes. Antenna 1 peduncle article 1 with 1 lateral robust seta. Antenna 2 peduncle article 3 with 1 pair of robust setae; article 4 with row of 3 single robust setae, without Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 89 First record of Monocorophium uenoi in the Bay of Biscay distoventral tooth; article 5 without proximoventral process and with 1 ventromedial robust seta. Figure 2. Monocorophium uenoi (Stephensen, 1932), males specimens from Jacquet, Arcachon Bay, July 2014. A) Head and antenna dorsal view; B) antenna 1 article 1 mesial view; C) antenna 2 mesial view with article 4 proximal ventromedial robust seta (black arrow); D) antenna 2 article 4 distoventral teeth and article 5 proximal ventral process (black arrow); E–G) gnathopod 2 distal part of propodus and dactylus showing variability in dactylus teeth; H) gnathopod 1 distal part of propodus and dactylus; I) uropod 1 and 2 dorsal view; J) telson dorsal view. Scale bars: A–C, I: 0.2 mm; D–H, J: 0.05 mm. Photomicrographs by B. Gouillieux. Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 90 First record of Monocorophium uenoi in the Bay of Biscay Figure 3. Monocorophium uenoi (Stephensen, 1932), females specimens from Jacquet, Arcachon Bay, July 2014; A) antenna 1 article 1 mesial view; B) antenna 2 mesial view; C) urosome dorsal view. Monocorophium acherusicum (Costa, 1853), specimens from Arcachon Bay; D) male antenna 1 article 1 mesial view; E) male antenna 2 mesial view; F) female antenna 2 mesial view; G) uropod 1 dorsal view. Monocorophium insidiosum (Crawford, 1937), male specimens from Bidasoa Estuary; H) head and antenna dorsal view showing medial process on antenna 1 article 1 (black arrow). Monocorophium sextonae (Crawford, 1937), male specimen from Arcachon Bay; I) antenna 1 article 1 mesial view; J) antenna 2 mesial view. Scale bars: A, D: 0.1 mm; B, C, E–J: 0.2 mm. Photomicrographs by B. Gouillieux. Variability Based on 60 specimens from Arcachon Bay and Bidasoa Estuary (BL range: 1.7–6.2 mm). Antenna 1 peduncle article 1 with 0–2 (7%) or 3–4 (93%) ventral robust setae. Antenna 2 peduncle article 4 with (80%) or without (20%) ventromedial Gouillieux and Massé (2019), BioInvasions Records 8(1): 87–95, https://doi.org/10.3391/bir.2019.8.1.09 91 First record of Monocorophium uenoi in the Bay of Biscay robust setae. Gnathopod 2 dactylus with 2 (13%) or 3 (74%) teeth, or with no left/right symmetry (13%), third tooth sometimes difficult to see (Figure 2F). Number of robust setae on antenna 1 peduncle article 1 or number of gnathopod 2 dactylus teeth not significantly correlated to body length (Spearman, ρ = 0.22; p-value = 0.1) Discussion Description of Monocorophium uenoi Monocorophium uenoi present specimens correspond to Stephenson (1932) and subsequent descriptions except for: (1) female antenna 1 article 1 with 1 medial robust seta (versus 4 or 5 for Nagata 1960); (2) female antenna 2 article 3 with 2 robust setae (versus 3 for Barnard 1952); (3) male antenna 2 peduncle article 5 with proximoventral process (versus without for Stephensen 1932 and Nagata 1960; with or without for Barnard 1952); (4) gnathopod 2 dactylus with 2 or 3 posterior teeth (versus 3 or 4 for Faasse 2014); (5) telson with 3 proximolateral setae and with 2 row of 4 robust setae tooth-like on the dorsodistal depression (versus 1 pair of proximolateral setae and 2 row of 3 robust setae tooth-like for Stephensen 1932).